Stronger Historical Contingency Facilitates Ecological Specializations: An Example with Avian Carotenoid Networks

AbstractEvolution requires both robustness of adaptive states and transitions between them. Understanding the mechanisms that reconcile these seemingly opposing properties is limited by the transient nature of evolutionary processes, where past pathways and contexts are often lost. Here, we overcome this limitation by tracing the biochemical evolution of avian carotenoid networks on the global carotenoid biochemical network, which is unmodified in avian evolution. By mapping enzymatic interactomes of 260 extant bird species and their reconstructed ancestral states onto this global network, we reveal that stepping stones between them are evolutionarily stable degenerate carotenoids-compounds that can be synthesized interchangeably by different dietary carotenoid-specific pathways. We find that ecological specialization across taxonomic groups is consistently associated with an uneven biochemical reach of individual dietary carotenoids, leading to increased fragmentation and reduced resilience of enzymatic networks to failure. However, the robustness of enzymatic networks of specialized groups is restored by the accumulation of degenerate carotenoids. This accumulation enables direct transitions between ecological specializations and sustains evolutionary explorations. Thus, the same feature of network structure-its degeneracy-increases the robustness of specialized enzymatic networks as enables evolutionary transitions between them. These findings provide an insight into the mechanistic basis for the interplay between natural selection and historical contingency, highlighting their fundamental interdependence.